Coelenterate Biology 2003 Developments in Hydrobiology 178

Series editor K. Martens Coelenterate Biology 2003 Trends in Research on and Ctenophora Proceedings of the 7th International Conference on Coelenterate Biology, held at the University of Kansas, Lawrence, Kansas, U.S.A., 6–11 July 2003

Edited by D.G. Fautin1, J.A. Westfall2, P. Cartwright1, M. Daly3 & C.R. Wyttenbach1

1University of Kansas, U.S.A. 2Kansas State University, U.S.A. 3University of Kansas, U.S.A. (currently Ohio State University, U.S.A.)

Reprinted from Hydrobiologia, volumes 530/531 (2004)

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Printed in the Netherlands TABLE OF CONTENTS

Introduction and Acknowledgments xi–xiii

PART I: PIONEERS IN COELENTERATE BIOLOGY Charles McLean Fraser (1872–1946) – his contributions to hydroid research and to the development of fisheries biology and academia in British Columbia M.N. Arai 3–11 From birds to hydroids: Charles Cleveland Nutting (1858–1927) of the University of Iowa, USA D.R. Calder 13–25 The first description of nerves in a cnidarian: Louis Agassiz’s account of 1850 G.O. Mackie 27–32

PART II: NEUROBIOLOGY + Introduction to the Symposium 33 Biogenic amine receptors in the sea pansy: activity, molecular structure, and physiological significance M. Anctil, C. Bouchard 35–40 Chemical anatomy of hydra nervous system using antibodies against hydra neuropeptides: a review O. Koizumi, N. Sato, C. Goto 41–47 Neuropeptides and photic behavior in Cnidaria G. Plickert, B. Schneider 49–57 Different roles of GABA and glycine in the modulation of chemosensory responses in Hydra vulgaris (Cnidaria, ) P. Pierobon, A. Tino, R. Minei, G. Marino 59–66 Glutamatergic and GABAnergic control in the tentacle effector systems of Hydra vulgaris G. Kass-Simon, A.A. Scappaticci, Jr. 67–71 Epithelial conduction: recent findings, old questions, and where do we go from here? G.O. Mackie 73–80 Impulse conduction in the jellyfish digitale R.W. Meech 81–89 Spasm behavior and the diffuse nerve-net in Cassiopea xamachana (Scyphozoa: Coelenterata) L.M. Passano 91–96 Mechanoreception and synaptic transmission of hydrozoan nematocytes U. Thurm, M. Brinkmann, R. Golz, M. Holtmann, D. Oliver, T. Sieger 97–105 Cnidarian neurobiology: what does the future hold? P.A.V. Anderson 107–116 Neural pathways and innervation of cnidocytes in tentacles of sea anemones J.A. Westfall 117–121 vi

Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation G.M. Watson, P. Mire 123–128 The photobiology of Hydra’s periodic activity C. Taddei-Ferretti, C. Musio, S. Santillo, A. Cotugno 129–134 Photoreceptors of cubozoan jellyfish V.J. Martin 135–144 A mechanosensory system that controls feeding in adult Mnemiopsis A.G. Moss, B. Wells, L. Muellner 145–153 Primary inhibition: a mechanism for sudden stoppage of metachrony in ctenophores A.G. Moss 155–162

PART III: CNIDAE Nematocysts of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes A. Ibragimov, E. Raikova 165–171 Nematocyst composition of the cubomedusan Chiropsalmus quadrigatus changes with growth A. Oba, M. Hidaka, S. Iwanaga 173–177 A review of zoanthid nematocyst types and their population structure J.S. Ryland, J.E. Lancaster 179–187 Variability in nematocysts from a single individual of the sea anemone Actinodendron arboreum (Cnidaria: Anthozoa: Actiniaria) A. Ardelean, D.G. Fautin 189–197 Hydroid nematophores: morphological, structural, and behavioural variety from old knowledge and new data N. Gravier-Bonnet 199–208 PART IV: & SYSTEMATICS Use of X-radiographs to distinguish members of the Montastraea annularis reef-coral complex M. Holcomb, J.M. Pandolfi, I.G. Macintyre, A.F. Budd 211–222 Redescription of Bedotella armata from Biscay Bay, northern Spain, the type species of Bedotella Stechow, 1913 (Cnidaria, Hydrozoa, Lafoeidae), with comments on its taxonomic position A.C. Marques, A. Altuna, A.L. Pen˜a Cantero, A.E. Migotto 223–230 First full description of the large physonect siphonophore Halistemma amphytridis (Lesueur & Petit, 1807) G.M. Mapstone 231–240 Phylogeny and biogeography of Anthopleura in the North Atlantic Ocean M. Daly 241–248 Some implications of molecular phylogenetics for understanding biodiversity in jellyfishes, with emphasis on Scyphozoa M. N Dawson 249–260 vii

On the taxonomy and presumable evolutionary pathways of planktonic larvae of Ceriantharia (Anthozoa, Cnidaria) T.N. Molodtsova 261–266 Cloning and sequencing of cDNA encoding glutamine synthetase from the sea anemone Aiptasia pallida O.P. Smith, A.D. Marinov, K.M. Chan, M.D. Ferrier 267–272

PART V: AXIAL PATTERNING The dynamics of multiple mouth formation in Fungia granulosa: possible patterning mechanisms V. Jacoby, E. Kramarsky-Winter, Y. Loya, O. Mokady 275–281 Evolution and dynamics of branching colonial form in marine modular cnidarians: gorgonian octocorals J.A. Sa´nchez 283–290 The role of polyp-stolon junctions in the redox signaling of colonial hydroids N.W. Blackstone, K.S. Cherry, D.H. Van Winkle 291–298 Variations on a theme? Polyp and medusa development in Podocoryna carnea D.M. Bridge, C.T. Ha, A. Nemir, A. Renden, M.M. Rorick, A. Shaffer, D.M. Underkoffler, A.E. Wills, D.E. Martı´nez 299–307 The development and evolution of hydrozoan polyp and colony form P. Cartwright 309–317 Morphogenetic evolution of hydroid colony pattern N.N. Marfenin, I.A. Kosevich 319–327

PART VI: REPRODUCTION, DEVELOPMENT, LIFE CYCLES Budding, bud morphogenesis, and regeneration in Carybdea marsupialis Linnaeus, 1758 (Cnidaria: Cubozoa) A.B. Fischer, D.K. Hofmann 331–337 Growth and age determination of the tropical Australian cubozoan Chiropsalmus sp. M. Gordon, C. Hatcher, J. Seymour 339–345 The life cycle of Chrysaora lactea Eschscholtz, 1829 (Cnidaria, Scyphozoa) with notes on the scyphistoma stage of three other species A.C. Morandini, F.L. da Silveira, G. Jarms 347–354

D-Methionine and gold chloride alleviate adverse eects of glutamate on motility of ephyrae of Aurelia aurita (Linnaeus, 1758) (Scyphozoa: Semaeostomeae) D.B. Spangenberg, F.A. Lattanzio, G. Navarro 355–363 Medusoid release and spawning of Macrorynchia philippina Kirchenpauer, 1872 (Cnidaria, Hydrozoa, Aglaopheniidae) C. Bourmaud, N. Gravier-Bonnet 365–372 Gonad development and somatic growth patterns of Olindias sambaquiensis (Limnomedusae, Olindiidae) L. Chiaverano, H. Mianzan, F. Ramı´rez 373–381 viii

Reproduction of the colonial hydroid Obelia geniculata (L., 1758) (Cnidaria, Hydrozoa) in the White Sea S.A. Slobodov, N.N. Marfenin 383–388 Heterogeneous and compensatory growth in Melithaea flabellifera (Octocorallia: Melithaeidae) in Japan A.K. Matsumoto 389–397 Reproduction and the unusual condition of hermaphroditism in Sarcophyton glaucum (Octocorallia, Alcyoniidae) in KwaZulu-Natal, South Africa M.H. Schleyer, A. Kruger, Y. Benayahu 399–409 The reproductive biology of Parazoanthus parasiticus (Hexacorallia: Zoanthidea) in Bermuda J.S. Ryland, D. Westphalen 411–419

PART VII: CORAL REEFS Morphological and genetic variation across reef habitats in a broadcast-spawning octocoral E. Kim, H.R. Lasker, M.A. Coffroth, K. Kim 423–432 Demographic aspects of the soft coral Sinularia flexibilis leading to local dominance on coral reefs C. Bastidas, K.E. Fabricius, B.L. Willis 433–441 Allorecognition and xenorecognition in reef corals: a decade of interactions B. Rinkevich 443–450 Epidermal structure of the scleractinian coral Mycetophyllia ferox: light-induced vesicles, copious mucocytes, and sporadic tentacles W.M. Goldberg 451–458 Adaptive bleaching: a general phenomenon D.G. Fautin, R.W. Buddemeier 459–467 Observations of a new source of coral mortality along the Kenyan coast T.R. McClanahan, S.M. McLaughlin, J.E. Davy, W.H. Wilson, E.C. Peters, K.L. Price, J. Maina 469–479 Coral mortality, recovery and reef degradation at Mexico Rocks Patch Reef Complex, Northern Belize, Central America: 1995–1997 C.D. Burke, T.M. McHenry, W.D. Bischoff, E.S. Huttig, W. Yang, L. Thorndyke 481–487 Synoptic water clarity assessment in the Florida Keys using diffuse attenuation coefficient estimated from Landsat imagery D. Palandro, C. Hu, S. Andre´foue¨t, F.E. Muller-Karger 489–493

PART VIII: ECOLOGY Distribution of sea anemones (Cnidaria, Actiniaria) in Korea analyzed by environmental clustering H.-R. Cha, R.W. Buddemeier, D.G. Fautin, P. Sandhei 497–502 Description and ecology of Cytaeis capitata n. sp. (Hydrozoa, Cytaeididae) from Bunaken Marine Park (North Sulawesi, Indonesia) S. Puce, A. Arillo, C. Cerrano, R. Romagnoli, G. Bavestrello 503–511 ix

Effects of anemonefish on giant sea anemones: expansion behavior, growth, and survival D. Porat, N.E. Chadwick-Furman 513–520 Predation of freshwater jellyfish on Bosmina: the consequences for population dynamics, body size, and morphology T. Jankowski 521–528 Associations between gelatinous zooplankton and hyperiid amphipods (Crustacea: Peracarida) in the Gulf of California R. Gasca, S.H.D. Haddock 529–535 The scyphomedusan fauna of the Japan Trench: preliminary results from a remotely- operated vehicle D.J. Lindsay, Y. Furushima, H. Miyake, M. Kitamura, J.C. Hunt 537–547 A golden age of gelata: past and future research on planktonic ctenophores and cnidarians S.H.D. Haddock 549–556 Index 557–565 Hydrobiologia 530/531: xi–xiii, 2004. xi D.G. Fautin, J.A. Westfall, P. Cartwright, M. Daly & C.R. Wyttenbach (eds), Coelenterate Biology 2003: Trends in Research on Cnidaria and Ctenophora.

Introduction and acknowledgements

This volume is organized, as was the Seventh part of the Axial Patterning symposium, constitute International Conference on Coelenterate Biology, that section. Papers deal with pattern formation around six themes. All but one of the contribu- both within individuals and in the colonies that tions on neurobiology were part of a symposium many of our marvelously varied form. on that subject. Some of the contributions on Attention to detail is also evident in the closely- Reproduction, Development, and Life Cycles were related section on Reproduction, Development, part of the symposium on Axial Patterning. Pio- and Life Cycles. All four classes of Cnidaria are neers in Coelenterate Biology was the subject of a represented among those 11 papers; three of them special session. Contributed papers organized deal with the seldom-studied Cubozoa. Martin- around the theme of Ecology included those on dale’s plenary address and Boero’s banquet talk Coral Reefs, which constituted the 2003 North (neither of which is published in this volume) American meeting of the International Society for converged on the idea that cnidarians are, deep Reef Studies (ISRS). The other two themes were down, bilateral and triploblastic, a theme that was Cnidae, and Taxonomy and Systematics. echoed in some of developmental papers in the Three of the five presentations made in the volume. session on Pioneers in Coelenterate Biology are Of the presentations on Coral Reefs that ex- published here. They provide a wonderful glimpse tended through much of a day and a half, eight are into the world of our science from the mid-19th published here. As is true of reefs themselves, the century to the mid-20th century. Mary Arai de- theme of variability is very much in evidence. As a scribes the career of her countryman Fraser. Dale sad sign of the times, half of them deal with effects Calder’s account shows that having an ICCB7 in of stress in the animals or detecting stress in the the middle of North America is not so strange, environment. The rest of the papers concerning following as it does in the tradition of Nutting. Ecology run the gamut from freshwater to the And George Mackie’s vindication of Louis Agas- deep sea, and include the only plenary address in siz’s observations provide an ideal segue to the the volume, Haddock’s reflections on research on Symposium on the Neuroanatomy and Neuro- planktonic coelenterates. physiology of Coelenterates. The organizers of ICCB7 were repeatedly The symposium has its own introduction, challenged about using the term ‘coelenterate.’ The which summarizes the contents of the 15 papers reason for doing so is two-fold: for continuity of a presented in it, and highlights the variability in tradition (see history below) and for inclusiveness, coelenterates that makes them so interesting and as I have just used it, to cover ctenophores (about challenging to study. The sine qua non of cnidari- which there were several presentations) as well as ans, cnidae, continue to provide grist for our re- cnidarians. search mill. A theme of two of the papers about them in this volume is also variability – its extent in species and individuals. Other techniques ap- Narrative of conference and acknowledgments plied to sorting out cnidarians and their relation- ships constitute the section on Taxonomy and ICCB7 was held 6–11 July 2003 at the University Systematics. They range from x-rays to molecules, of Kansas (KU), Lawrence, Kansas, USA. It and show there is no substitute for the time-hon- began with a reception the evening of Sunday, 6 ored and time-consuming practice of detailed July, at the University of Kansas Natural History observation. Five of the 13 presentations in the Museum. Sessions were held all day Monday, symposium, plus one that one was not given as Tuesday, and Thursday, and the morning of Fri- xii day the 11th. The meeting was followed by two tional, ISRS, Free State Brewery (Lawrence), days of workshops. In addition to the welcome Ray’s Liquor, HyVee, Office Depot, and H. Stevan reception, social events included a Kansas barbe- Logsdon, wildlife artist. que Tuesday evening and a banquet Thursday Special thanks are due to people who provided evening. Field trips were held on Wednesday. logistical help. Registration, arrangements for The 197 registrants presented 139 oral presen- space and transportation, etc. was handled by tations and 67 posters. A plenary talk was given Sharon Brookshire, assisted by Ellen Stauffer and each meeting day. They were, in sequence, Rebeccas Frakes of the Division of Continuing ‘Glowing gelata: bioluminescence and biodiversity Education, Kansas State University. Coordinating of deep-sea ctenophores and cnidarians’ by Steven facilities at the Kansas Union was Lisa Kring. H. D. Haddock, ‘Reefs and organisms change but Audio-visual services were by Ganesh Shankaran, the play goes on: a billion years of reef evolution’ assisted by Asif Iqbal, John Guinotte, and Kai by George D. Stanley, Jr., ‘Cnidarians: degenerate Raab. Transportation and barbeque arrangements triploblastic bilateralians’ by Mark Q. Martindale were by Lorraine Murtha. The barbeque was at (with co-authors Kevin Pang, Pat Burton, and Pendleton’s Country Market and Farm, the chief John R. Finnerty), and ‘The symbiotic condition: cook was Joe Markley, chickens were grown at the role of algae in cnidarian hosts’ by Gisle Muller- Clark Family Farms, bison was raised by Lone Parker. The banquet talk presented, virtually, by Star Lake Bison Ranch and Meat Company, pies Ferdinando Boero was ‘Born to be triploblastic – and rolls were made by MMMS Baked Goods and bilateral.’ The symposium ‘Neurobiology,’ (Mary, Margaret, Molly, and Sarah), and beer was organized by Jane Westfall, was held Monday and from the Free State Brewery. Tuesday, and the symposium ‘Axial patterning,’ organized by Paulyn Cartwright, was held Thurs- day. The special session ‘Pioneers in Coelenterate Proceedings Biology’ was held Friday morning. The Organizing Committee of ICCB7 con- In addition to the contribution of registration fees sisted of Daphne G. Fautin (Chair) (KU), Ann to the production of this volume, US NSF grant F. Budd (University of Iowa), Robert W. Bud- IBN02-44459 to Jane Westfall helped pay for demeier (Kansas Geological Survey), Matthew publication of papers that were part of the sym- Buechner (KU), Paulyn Cartwright (KU), posium ‘Neuroanatomy and Neurophysiology of Marymegan Daly (KU), Paul Enos (KU), Jane Coelenterates.’ Ganesh Shankaran as well as stu- Westfall (Kansas State University), and Charles dents employed through Sloan Foundation funds Wyttenbach (KU). awarded through the Census of Marine Life The major financial contributors to ICCB7 helped with the logistics of compiling the volume were the US National Science Foundation, which manuscripts. provided grants to Daphne Fautin (DEB99-78106 and a supplement to it), Jane Westfall (IBN02- 44459), and Paulyn Cartwright (333110), and Al- len Press (which is located in Lawrence). Units of Previous ICCBs and resulting volumes KU that contributed financially and in kind to ICCB7 were the Center for Research, Inc., the 3–4 March 1965 – The Zoological Society of Department of Ecology and Evolutionary Biology, London, UK the Department of Geology, the Department of Organizing Committee: W. J. Rees (chair), Sir Molecular Biosciences, the Kansas Geological Fredrick Russell, C. F. A. Pantin, Cadet Hand, D. Survey, KU Bookstores, and the Natural History M. Ross. Museum and Biodiversity Research Center. Other Number of Attendees: 27 contributors and sponsors were Eastman Kodak Proceedings: Rees, W. J. (ed.), 1966. The Company Scientific Imaging Systems, SpaceSaver/ Cnidaria and their Evolution. Symposia of the Delta Designs, Hitschfel Instruments, Fisher Sci- Zoological Society of London 16. London: Aca- entific, VWR International, Nalge Nunc Interna- demic Press. 449 pages. xiii

16–19 October 1972 – Shirahama and Kushimoto, 10–14 July 1989 – University of Southampton, UK Japan Organizing Committee: R. G. Hughes (chair), Organizing Committee: Tohru Uchida (chair), P. F. S. Cornelius, E. A. Robson, M. A. Carter, J. A. Brinckmann-Voss, G. O. Mackie, W. A. Mu¨l- A. E. B. Hubbard, R. B. Williams ler, D. M. Chapman, S. Kawaguti, H. R. Randall, Number of Attendees: 250 C. Edwards, H. Thiel, L. M. Passano, M. Tam- Proceedings: Williams, R. B., P. F. S. Corne- asige, R. Weill, M. N. Arai, E. A. Robson, E. lius, R. G. Hughes & E. A. Robson (eds), 1991. Harada, M. Yoshida, D. Ross Coelenterate Biology: Recent Research on Cnidaria Number of Attendees: 46 and Ctenophora. Boston: Kluwer Academic Pub- Proceedings: Tokioka, Takasi (ed.), 1973. Re- lishers. 742 pages. cent Trends in Research in Coelenterate Biology. Publications of the Seto Maine Biological Labo- 16–21 July 1995 – The Leeuwenhorst Conference ratory 20. 793 pages. Center, Noordwijkerhout, The Netherlands Organizing Committee: S. van der Spoel (chair), 10–13 May 1976 – University of Victoria, Victoria, R. M. L. Ates, J. Bleeker, J. C. den Hartog, J. H. BC, Canada M. Kouwenberg, A. C. Pierrot-Bults, P. H. Organizing Committee: George O. Mackie Schalk, R. W. M. van Soest, H. W. van der Veer, (chair), Mary Needler Arai, Donald M. Ross J. Vermeulen Number of Attendees: 139 Number of Attendees: 130 Proceedings: Mackie, G. O. (ed.), 1976. Coel- Proceedings: den Hartog, J. C., L. P. van enterate Ecology and Behavior. New York: Plenum Ofwegen & S. van der Spoel (eds), 1997. Pro- Press. 744 pages. ceedings of the 6th International Conference on Coelenterate Biology. Leiden, The Nether- 4–8 September 1979 – Interlaken, Switzerland lands: Nationaal Naturhistorisch Museum. 542 Organizing Committee: Pierre Tardent, Ruth pages. Tardent (co-chairs), staff members and students of the Zoological Institute of the University of Zu¨rich Number of Attendees: 109 Proceedings: Tardent, P. & R. Tardent (eds), 1980. Developmental and Cellular Biology of Coelenterates. Amsterdam: Elsevier/North Hol- land Biomedical Press. 499 pages.